Adam R. Reddon

Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task

Animal personality, defined as consistent individual differences across context and time, has attracted much recent research interest in the study of animal behaviour. More recently, this field has begun to examine how such variation arose and is maintained within populations. The habitat-dependent selection hypothesis, which posits that animals with differing personality types may fare better (i.e. have a fitness advantage) in different habitats, suggests one possible mechanism. In the current experiment, we tested whether slow- and fast-exploring black-capped chickadees (Poecile atricapillus), determined by performance in a novel environment exploration task, perform differentially when the demands of an acoustic operant discrimination (cognitive) task were altered following successful task acquisition. We found that slow-exploring birds learn to reverse previously learned natural category rules more quickly than faster exploring conspecifics. In accordance with the habitat-dependent selection hypothesis, and previous work with great tits (Parus major), a close relative of the black-capped chickadee, our results suggest that fast-exploring birds may perform better in stable, predictable environments where forming a routine is advantageous, while slow-exploring birds are favoured in unstable, unpredictable environments, where task demands often change. Our results also support a hypothesis derived from previous work with great tits; slow-exploring birds may be generally more flexible (i.e. able to modify their behaviour in accordance with changes in environmental stimuli) in some learning tasks.

Exploration of a novel space is associated with individual differences in learning speed in black-capped chickadees, Poecile atricapillus

Individual variation in exploratory behaviour has been demonstrated in a diverse array of animal species. Understanding the evolutionary antecedents and ecological consequences of this variation is an active research area within animal behaviour. Here we investigate whether different exploration styles exhibited by black-capped chickadees (Poecile atricapillus) in a novel environment are related to how quickly these birds learn an acoustic discrimination task. We found that birds that readily enter a novel environment learn an acoustic discrimination task faster than birds that do not readily enter a novel environment. This result contrasts with previous work suggesting no correlation between exploration style and learning a spatial or associative task in great tits (Parus major), a close relative of the black-capped chickadee.

Aggression, sex and individual differences in cerebral lateralization in a cichlid fish

Cerebral lateralization is an evolutionarily ancient adaptation, apparently ubiquitous among vertebrates. Despite demonstrated advantages of having a more lateralized brain, substantial variability in the strength of lateralization exists within most species. The underlying reasons for the maintenance of this variation are largely unknown. Here, we present evidence that the strength of lateralization is linked to a behavioural trait, aggressiveness, in the convict cichlid (Archocentrus nigrofasciatus), and that this relationship depends on the sex of the fish. This finding suggests that individual variation in behaviour may be linked to variation in cerebral lateralization, and must be studied with regard to the sex of the animal.

Individual differences in cerebral lateralization are associated with shy–bold variation in the convict cichlid

Cerebral lateralization, the preferential use of one hemisphere of the brain to perform certain cognitive functions, is a widespread and evolutionarily ancient adaptation. Lateralization appears to enhance cognitive capacity, yet substantial individual variation in the strength cerebral lateralization is apparent in all species studied so far. It is puzzling that cerebral lateralization, a seemingly advantageous trait, has not been driven to fixation. It has been suggested that variation in lateralization may be linked to individual variation in behaviour, which itself may be subject to disruptive selection. We examined the relation between cerebral lateralization and individual variation in boldness in the convict cichlid, Archocentrus nigrofasciatus . We show that convict cichlids that are more strongly lateralized when exploring a familiar environment, but not a novel one, are quicker to emerge from a shelter in a test for boldness. The possibility that cerebral lateralization is linked to life history strategy is discussed.

Is there a role for aggression in round goby invasion fronts

The role of aggression as a factor promoting invasiveness remains hotly debated. Increased aggression or a lack of tolerance for conspecifics may promote population spread. Some previous research suggests that more aggressive or bold individuals are increasingly likely to disperse and as such these individuals may be overrepresented at the invasion front. In contrast, it has also been argued that individuals at the invasion front represent the least aggressive or least competitive individuals in the population, as these animals are excluded from established areas. Accordingly, the invasion front should be made up of shy, submissive individuals that exhibit reduced aggression. In this study we explore these alternative predictions by quantifying the levels of intra-specific aggression in the round goby (Neogobius melanostomus), an invasive fish that continues to spread rapidly through the Laurentian Great Lakes region in North America. We collected size matched male round goby from an invasion front as well as from an area with an established population, and we staged resource contests between them. Invasion front fish won 65% of the contests and tended to perform more aggressive acts overall. Invasion front fish were not more active or bold prior to the contest, and used the same types of aggressive displays as fish from established areas. Our results also showed that body size asymmetry was an overriding determinant of competitive outcomes, and that body size rather than individual variation in aggressiveness might be the most important contributing factor determining the composition of round goby invasion fronts throughout the Laurentian Great Lakes and its tributaries.

The relationship between growth, brain asymmetry and behavioural lateralization in a cichlid fish

Cerebral lateralization, the partitioning of cognitive tasks to one cerebral hemisphere, is a widespread phenomenon among vertebrates. Despite this diversity, every species studied to date shows substantial individual variation in the strength of lateralization. The neural basis of this trait is unclear, although asymmetries in cerebral structures have been investigated for over a century. The habenular nuclei, for example, have been shown to present striking neuroanatomical and/or neurochemical asymmetries in species ranging from jawless fish to mammals. In teleost fish, these nuclei are relatively symmetrical in most species. Those teleosts that do have asymmetrical habenular nuclei, show varying patterns of asymmetry in different species. Here we investigate the relationship between individual variation of asymmetry in the habenula of a South American cichlid fish, Geophagus brasiliensis, and behaviour in a commonly used test for visual laterality in fish, the detour task. We show that the strength of asymmetry in the habenula is correlated with strength of behavioural lateralization in the detour task. Both the strength and direction of habenular asymmetry are correlated with individual differences in growth rate. We suggest that this relationship results from processes linking growth rate and sexual differentiation to frequency-dependent variation in life-history strategies. To our knowledge, this is the first study to demonstrate a relationship at the individual level between neural asymmetry and lateralized behaviour in a fish.

Sex differences in the cerebral lateralization of a cichlid fish when detouring to view emotionally conditioned stimuli

The lateralization of emotion has been described in a variety of animals. The right hemisphere has been implicated in the processing of negative emotions while positive emotions are processed in the left. Most animal studies of this phenomenon to date have used intrinsically emotionally arousing stimuli and there are few examples of lateralized responses to learned emotional triggers. It is known that males and females may demonstrate different patterns of lateralization, and that these sex differences may interact with other variables. We investigated the lateralized response of male and female convict cichlids to emotionally conditioned stimuli. One stimulus was given an appetitive (positive emotional valence) association by pairing with food. The other stimulus was given an aversive (negative emotional valence) association by pairing with a chemical alarm signal. We found that males tend to be more strongly lateralized to aversive stimuli while females are more strongly lateralized when responding to appetitive stimuli.

Variation in asymmetry of the habenular nucleus correlates with behavioural asymmetry in a cichlid fish

Asymmetries in brain and behaviour have been demonstrated in numerous species representing all major vertebrate taxa, and may be a universal feature of the vertebrate nervous system. While descriptions of lateralization at the behavioural and neuroanatomical level are widespread, examples of correlation between asymmetries in behaviour and neural structures remain relatively scarce. In the past few years, the habenular nucleus has emerged as a potential site for the neural basis of some lateralized behaviours. Here we investigate the relation between continuous individual variation in asymmetry of the habenulae and behaviour in the detour task in the convict cichlid (Amatitlania nigrofasciata). We found that both male and female convicts show a significant population-level bias towards relatively larger left habenulae. We also show that habenular asymmetry is correlated with behavioural lateralization in both males and females, but in opposite directions. This adds to previous studies showing both in convict cichlids and other vertebrates an interaction between sex and lateralized behaviour. The results of this study increase our understanding of the role of the habenula in lateralized behaviour and highlight the importance of a comparative approach to understanding the development and evolution of habenular asymmetry.

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.

Brain nonapeptide levels are related to social status and affiliative behaviour in a cooperatively breeding cichlid fish.

The mammalian nonapeptide hormones, vasopressin and oxytocin, are known to be potent regulators of social behaviour. Teleost fishes possess vasopressin and oxytocin homologues known as arginine vasotocin (AVT) and isotocin (IT), respectively. The role of these homologous nonapeptides in mediating social behaviour in fishes has received far less attention. The extraordinarily large number of teleost fish species and the impressive diversity of their social systems provide us with a rich test bed for investigating the role of nonapeptides in regulating social behaviour. Existing studies, mostly focused on AVT, have revealed relationships between the nonapeptides, and both social behaviour and dominance status in fishes. To date, much of the work on endogenous nonapeptides in fish brains has measured genomic or neuroanatomical proxies of nonapeptide production rather than the levels of these molecules in the brain. In this study, we measure biologically available AVT and IT levels in the brains of Neolamprologus pulcher, a cooperatively breeding cichlid fish, using high performance liquid chromatography with fluorescence detection. We found that brain AVT levels were higher in the subordinate than in dominant animals, and levels of IT correlated negatively with the expression of affiliative behaviour. We contrast these results with previous studies, and we discuss the role the nonapeptide hormones may play in the regulation of social behaviour in this highly social animal.